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Re-modeling Chara action potential: I. from Thiel model of Ca2+transient to action potential form

1 School of Physics, University of NSW, Kensington, NSW 2052, Australia
2 Mathematics and Statistics, Western Sydney University, Bankstown, NSW 2200, Australia

Special Issues: BIOPHYSICS OF ION TRANSPORT IN PLANTS

Thiel and colleagues demonstrated that the all-or-none nature of Chara action potential(AP) is determined by formation of a second messenger, probably inositol triphosphate (IP3), whichin turn releases Ca2+ from internal stores. The Ca2+-activated Cl channels are the main agent of thedepolarization phase of the AP. Once the Ca2+ is re-sequestered by the calcium pumps, the chlorideconductance drops and depolarization-activated outward rectifier current, the background current andthe proton pump current return the membrane potential difference (PD) to resting level. Departingfrom the Thiel model of transient increase of Ca2+ concentration, we set up membrane PD rate ofchange equation to calculate the AP form by numerical integration. Compared to data, this model APdepolarized more gradually. We introduced a prompt Ca2+ transient from the outside, achieving agood correspondence with the experimental AP. In Chara cells subjected to 50 mM NaCl/0.1 mMCa2+ medium, the AP duration increased from 2 s to up to 50 s and the APs were often spontaneous.The lack of stimulating pulse revealed a sharp positive spike at the beginning of each AP, confirmingthat Chara plasma membrane may contain transient receptor potential (TRP)-like channels, possiblyactivated by another second messenger diacylglycerol (DAG) formed at the same time as IP3. Thelong duration of the saline AP can be modeled by decreasing the coefficients in the Hill equationdescribing the Ca2+ pumps on the internal stores. The model provides new insights into the characeanAP and suggests a range of experiments.
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References

1. Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117: 500–544.    

2. Beilby MJ (1976) An investigation into the electrochemical properties of cell membranes during excitation. School of Physics. University of New South Wales, Sydney, Australia, Doctor of Philosophy thesis

3. Beilby MJ, Coster HGL (1979a) The Action Potential in Chara corallina II. Two Activation-Inactivation Transients in Voltage Clamps of the Plasmalemma. Aust J Plant Physiol 6: 323–335.

4. Beilby MJ, Coster HGL (1979b) The Action Potential in Chara corallina III. The Hodgkin-Huxley Parameters for the Plasmalemma. Aust J Plant Physiol 6: 337–353.

5. Thiel G, MacRobbie EA, Hanke DE (1990) Raising the intercellular level of inositol 1,4,5-triphosphate changes plasma membrane ion transport in characean algae. EMBO J 9: 1737–1741.

6. Thiel G, Homann U, Plieth C (1997) Ion channel activity during the action potential in Chara: New insights with new techniques. J Exp Bot 48: 609–622.    

7. Kikuyama M, Shimada K, Hiramoto Y (1993) Cessation of cytoplasmic streaming follows an increase of cytoplasmic Ca2+ during action potential in Nitella. Protoplasma 174: 142–146.    

8. Biskup B, Gradmann D, Thiel G (1999) Calcium release from InsP3-sensitive internal stores initiates action potential in Chara. FEBS Let 453: 72–76.    

9. Wacke M, Thiel G (2001) Electrically triggered all-or-none Ca2+ liberation during action potential in the giant alga Chara. J Gen Physiol 118: 11–21.

10. Wacke M, Thiel G, Hutt MT (2003) Ca2+ dynamics during membrane excitation of green alga Chara: model simulations and experimental data. J Memb Biol 191: 179–192.    

11. Othmer HG (1997) Signal transduction and second messenger systems. In: Case studies in Mathematical Modeling—Ecology, Physiology and Cell Biology. Englewood Cliffs: Prentice Hall, 123–186.

12. Tazawa M, Kikuyama M (2003) Is Ca2+ released from internal stores involved in membrane excitation in characean cells? Plant Cell Physiol 44: 518–526.    

13. Shepherd VA, Beilby MJ, Al Khazaaly S, et al. (2008) Mechano-perception in Chara cells: the influence of salinity and calcium on touch- activated receptor potentials, action potentials and ion transport. Plant Cell Environ 31: 1575–1591.

14. Beilby MJ, Al Khazaaly S (2009). The role of H+/OH- channels in salt stress response of Chara australis. J Memb Biol 230: 21–34.

15. Al Khazaaly S, Beilby MJ (2012) Zinc ions block H+/OH- channels in Chara australis. Plant Cell Environ 35: 1380–1392.

16. Zherelova OM (1989) Activation of chloride channels in the plasmalemma of Nitella syncarpa by inositol 1,4,5-trisphosphate. FEBS Let 249: 105–107.    

17. Beilby MJ, Casanova MT (2013) The Physiology of Characean Cells. Berlin: Springer.

18. Hansen UP, Gradmann D, Sanders D, et al. (1981) Interpretation of current-voltage relationships for “active” ion transport systems: I. steady-state reaction-kinetic analysis of class-I mechanisms. J Memb Biol 63: 165–190.

19. Amtmann A, Sanders D (1999) Mechanisms of Na+ uptake by plant cells. Adv Bot Res 29: 75–112.

20. Beilby MJ, Walker NA (1996) Modelling the current-voltage characteristics of Chara membranes. I. the effect of ATP and zero turgor. J Memb Biol 149: 89–101.

21. Bush EW, Hood DB, Papst PJ, et al. (2006) Canonical transient receptor potential channels promote cardiomyocyte hypertrophy through activation of calcineurin signaling. J Biol Chem 281: 33487–33496.    

22. Trewavas A (1999) Le Calcium, C’est la Vie: Calcium Makes Waves. Plant Physiol 120: 1–6.    

23. Munnik T, Vermeer JE (2010) Osmotic stress-induced phophoinositide and inositol phosphate signalling in plants. Plant Cell Environ 33: 655–669.    

24. Tang RH, Han S, Zheng H, et al. (2007) Coupling diurnal cytosolic Ca2+ oscillations to the CAS?IP3 pathway in Arabidopsis. Science 315: 1423–1426

25. Perera IY, Heilmann I, Boss WF (1999) Transient and sustained increases in inositol 1,4,5-trisphosphate precede the differential growth response in gravistimulated maize pulvini. Proc Natl Acad Sci 96: 5838–5843.

26. Dong W, Lv H, Xia G, et al. (2012) Does diacylglycerol serve as a signaling molecule in plants? Plant Sign Behav 7: 472–475.    

27. Mikami K (2014) Comparative genomic view of the Inositol-1,4,5-trisphosphate receptor in plants. J Plant Biochem Physiol 2: doi:10.4172/2329-9029.1000132.

28. Lemtiri-Chlieh F, MacRobbie EA, Webb AA, et al. (2003) Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells. Proc Natl Acad Sci 100: 10091–10095.

29. Berestovsky GN, Kataev AA (2005) Voltage-gated calcium and Ca2+-activated chloride channels and Ca2+ transients: voltage-clamp studies of perfused and intact cells of Chara. Euro Biophys J 34: 973–986.    

30. Baudenbacher F, Fong LE, Thiel G, et al. (2005) Intracellular axial current in Chara corallina reflects the altered kinetics of ions in cytoplasm under the influence of light. Biophys J 88: 690–697.    

31. Wheeler GL, Brownlee C (2008) Ca2+ signaling in plants and green algae-changing channels. Trends Plant Sci 13: 506–514.    

32. Teakle NL, Tyerman SD (2010) Mechanisms of Cl transport contributing to salt tolerance. Plant Cell Environ 33: 566–589.    

33. Roelfsema M, Hedrich R (2010) Making sense out of Ca2+ signals: their role in regulating stomatal movements. Plant Cell Environ 33: 305–321.    

34. Hepler P (2005) Calcium: A central regulator of plant growth and development. Plant Cell 17: 2142–2155.    

Copyright Info: © 2016, Mary Jane Beilby, et al., licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution Licese (http://creativecommons.org/licenses/by/4.0)

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